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Ecology and Evolution of Facilitation Among Symbionts

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Ecology and Evolution of Facilitation Among Symbionts REVIEW ARTICLE DOI: 10.1038/s41467-018-06779-w OPEN Ecology and evolution of facilitation among symbionts Flore Zélé 1, Sara Magalhães 1, Sonia Kéfi 2 & Alison B. Duncan 2 Facilitation occurs when one species positively impacts the fitness of another, and has predominantly been studied in free-living species like plants. Facilitation can also occur among symbiont (mutualistic or parasitic) species or strains, but equivalent studies are 1234567890():,; scarce. To advance an integrated view of the effect of facilitation on symbiont ecology and evolution, we review empirical evidence and their underlying mechanisms, explore the factors favouring its emergence, and discuss its consequences for virulence and transmission. We argue that the facilitation concept can improve understanding of the evolutionary forces shaping symbiont communities and their effects on hosts. 1 cE3c: Centre for Ecology, Evolution, and Environmental Changes, Faculty of Sciences, University of Lisbon, Edifício C2, piso-3, 1749-016 Lisboa, Portugal. 2 ISEM, Université de Montpellier, CNRS, EPHE, IRD, Montpellier Cedex 05, France. Correspondence and requests for materials should be addressed to A.B.D. (email: [email protected]) NATURE COMMUNICATIONS | (2018)9:4869 | DOI: 10.1038/s41467-018-06779-w | www.nature.com/naturecommunications 1 REVIEW ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06779-w t is now widely accepted that interacting species can positively First, we outline the different mechanisms of impact one another1–5. Facilitation (Box 1) is one of the symbiont–symbiont facilitation. Next, we investigate the ecolo- Ibroadest terms referring to these positive interactions (Fig. 1). gical and evolutionary conditions favouring the occurrence and Its history is anchored in that of plant–plant interactions, maintenance of facilitation between symbiotic organisms. Finally, although its realm has recently been extended to include other we discuss the ecological and evolutionary consequences of taxa1. Studies to date generally document its occurrence, and the facilitation, and suggest future research avenues. Throughout, we ecological consequences of facilitation for individuals, species and highlight parallels with free-living organisms. ecosystems. The evolutionary causes and consequences of these 6 interactions, though tackled using modelling approaches and Mechanisms of facilitation phylogenetic analyses7, are still poorly assessed via contemporary 2 Symbionts can facilitate each other either directly (independently evolution studies . Despite the ubiquity of organisms that live of the host) or indirectly (via host manipulation) and facilitation within or upon others (endo or ecto-symbionts, hereafter ‘sym- can occur both within- and between-hosts (Fig. 2). Overall, the ’ bionts for brevity; Box 1), facilitation between symbionts has mechanisms of facilitation between symbionts are similar to those been largely overlooked. Indeed, individual hosts are often colo- found between free-living organisms (summarised in Fig. 3, along nised by multiple symbionts, which can have positive, negative or with some chosen examples; see also ref. 11, and Supplementary neutral effects on one another (Fig. 1), independently of their Table 1 for more examples of facilitation between symbionts). effect on the host (e.g. either parasitic, commensal or mutualistic). Symbiont–symbiont competition has been shown both empiri- cally and theoretically to have diverse effects on symbiont ecology Direct facilitation. Some symbionts directly facilitate the growth 8 or reproduction of others, by producing substances aiding them and evolution , but corresponding studies about facilitation in 12,13 multiple infections (Box 1) are lacking. The host-symbiont lit- to exploit the host (i.e. ‘supplied-product’ facilitation) . Direct – facilitation can occur when a symbiont facilitates another by erature contains many examples of symbiont symbiont interac- 14 tions compatible with facilitation (see Supplementary Table 1), affecting its gene expression (i.e. transactivation) or by pro- fi viding essential gene products such as in the case of transcapsi- though the interactions are rarely identi ed as such and are not 15 15,16 unified into a common body of work. Moreover, a number of dation or helper component-transcomplementation . Direct these studies investigate the evolutionary outcomes of facilita- facilitation can also arise when exogenous genetic material from 9,10 one symbiont becomes integrated in another (i.e. nested sym- tion , which may be relevant for the interpretation of ecological 17 patterns observed in both symbiotic and free-living systems. bionts) . Several reviews state that facilitative interactions have been relatively neglected in ecological theory, despite abundant Indirect facilitation. Within-host indirect facilitation can be empirical evidence for their occurrence in natural populations mediated by the modification of host resources used by sym- and indication of their importance for community functioning bionts18, or by improving host fitness in ways that benefit other and stability1,2,5. Here, we argue that facilitation has been parti- symbionts. For instance, by increasing host longevity, a symbiont cularly overlooked in the symbiont literature4. The aim of this can reduce the survival cost of infection by another parasite19, review is to highlight that integrating approaches used to study which, in turn enhances the probability that the latter completes facilitation in free-living organisms with studies of symbionts will its development within the host. be highly informative and beneficial for both fields of research. Indirect facilitation also occurs via the host immune system. On the one hand, placing symbiont–symbiont interactions in the This can be brought about by immune-evasion strategies such as context of facilitation should increase our understanding immunosuppression, which might be advantageous for other about infection outcomes. On the other hand, because it is symbionts within the host14, or via immunological trade-offs, easier to study evolution in symbionts than in most free-living whereby a host is unable to simultaneously mount immune organisms (given their shorter generation time), studies of responses against different symbionts20–22. Furthermore, sym- symbiont–symbiont facilitation may guide predictions about how bionts can facilitate host entry or exit of another4 via epidermal positive interactions between species could shape evolution in injuries23 or through the symptoms of infection24. free-living communities. Finally, behavioural or reproductive manipulation of the host by a symbiont can facilitate the transmission (Box 1) of other symbionts (e.g. ‘hitch-hiking’)25. This might occur between Commensalism horizontally transmitted symbionts with complex life cycles that share both intermediate and definitive hosts25, as well as between Facilitation symbionts with different transmission routes26 (Box 1). Vertically transmitted reproductive manipulators that increase the propor- +/0 tion of infected female offspring in the population27 can also facilitate the transmission of other vertically transmitted sym- bionts (i.e. via synergy or hitchhiking)27,28. Mutualism +/+ 0/0 Neutralism Multiple mechanisms and multiple effects Facilitation is often not easily attributed to a single mechanism. +/– 0/– For example, HIV-1 triggers lymphocyte activation, and activated –/– lymphocytes are the preferred resource of the human cytome- Antagonism Amensalism galovirus29. Hence, facilitation is immune-mediated from the facilitator perspective, but resource-mediated for the facilitated. Moreover, several facilitating mechanisms can operate simulta- Competition neously. For instance, the direct facilitation of polydnavirus Fig. 1 Diagram showing the different types of ecological interactions. 0: no transmission by parasitoid wasps described in Fig. 3 is accom- effect; –: negative effect; +: positive effect. Facilitation includes mutualistic, panied by an indirect facilitation by the virus for wasps, via commensal and antagonistic interactions silencing of the host immune system17. Importantly, many (if not 2 NATURE COMMUNICATIONS | (2018)9:4869 | DOI: 10.1038/s41467-018-06779-w | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06779-w REVIEW ARTICLE Box 1. Glossary Co-transmission: two or more symbionts are transmitted together, sometimes packaged together in the same protein case. Facilitation: any interaction where the action of one symbiont has a beneficial effect on another. This includes mutualistic interactions where both the facilitated and facilitator benefit(+/+), those which are commensal (+/0) when the effects of the facilitated on the facilitator are neutral as well as those which are antagonistic (+/−) when the facilitated negatively impact the facilitator (Fig. 1). Note that this concept partially overlaps with that of mutualism, ecological engineering and niche construction. Multiple infection: the presence of more than one symbiont (strain or species) circulating in an individual or population. Symbiont: As defined by Anton de Bary (1879): ‘the living together of unlike organisms’, we use this term to refer to any organism residing within or on hosts, encompassing all species along the mutualist–parasite continuum (i.e. they can be mutualists, commensalists or parasites of the host). Syntrophy: nutritional relationship between two organisms that combine their metabolic abilities to use a
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